Newly discovered mobile elements provide a means of rapid evolution of bacterium important in contaminant and metal fate and transport

Secondary structure of one of the three MITEs discovered in S. oneidensis MR-1. Enlarged View

Results: Researchers at Pacific Northwest National Laboratory recently mapped nearly 300 mobile elements within the genome of Shewanella oneidensis MR-1 and identified over 200 pseudogenes (genes with mutations predicted to prevent production of functional proteins), thereby advancing knowledge and understanding of the evolution of the bacterium. Mobile genetic elements are segments of DNA that can move within genomes through the action of enzymes (e.g., transposases, integrases, and recombinases) that either they encode or that are found elsewhere in the host in which they reside. These elements play an important role in the evolution of genomes by providing a means to get rid of unnecessary genetic baggage, eliminate or control expression of functions encoded by the host, or acquire new genetic material from other organisms that encode functions that are beneficial to the host, such as resistance to toxic materials.

S. oneidensis MR-1, an organism renowned for its remarkable broad respiratory capability, can respire ("breath") oxygen and, in the absence of oxygen, alternative compounds including metals and radionuclides. While the researchers' initial goal was to improve the annotation of its genome to facilitate ongoing studies aimed at characterizing the genetic basis for these abilities, their efforts led to several new discoveries that impact the understanding of how this organism has evolved and continues to evolve in response to changes in the environment in which it lives. It is possible, they suggest, that the many repetitions of a structural element within S. oneidensis MR-1 allow it to evolve much more rapidly than other bacteria.

Why it matters: The ability of bacteria to rapidly adapt to changes in their environment is essential to their survival, and by studying the consequences of their genome evolution one can learn more about how they have adapted to their environmental niches. Understanding the enhanced ability of S. oneidensis to acquire or evolve new functions advances fundamental knowledge of how to harness its potential ability to biologically change contaminants and affect contaminant fate and transport.

Currently, 20 genome sequences are available for Shewanella bacteria. All but one of these sequenced Shewanella strains can respire radionuclides. Several strains are able to degrade cyclotrimethylenetrinitramine (RDX), an explosive nitroamine widely used in military and industrial applications or halogenated ethenes, such as tetrachloroethene, which are widely used for the dry cleaning of fabrics.

Methods: The study approach used to map the mobile elements and identify the pseudogenes involved comparative analysis of genome sequences from multiple different Shewanella strains.

Using comparative analysis, researchers determined the locations of a common type of mobile element—the insertion sequence (IS) element—that encodes a transposase, and they found evidence that one of the 40 types of IS elements mapped also encodes an integrase, which supports it ability to capture foreign DNA by inserting it into the host DNA immediately adjacent to the IS element. They also discovered that MR-1 encodes another type of mobile element—a miniature inverted-repeat transposable element (MITE)—that does not encode the proteins necessary for its mobilization and has the propensity to form a cruciform structure (see figure). While MITEs are not self-mobilizing, evidence suggests that the three different types of MITEs discovered can be mobilized by transposases encoded elsewhere in the S. oneidensis genome.

What makes these findings even more unusual is that the mapping revealed a high number of identical copies of some of the mobile elements (up to 70 full-length copies of a single element). These repeated DNA regions can enable intrachromosomal homologous recombination, potentially resulting in deletion, duplication, translocation, and inversion of DNA within the genome, all of which can lead to the evolution of new genes and cellular functions that are beneficial to the host when it encounters a new environmental condition.

What's next: Follow-up research is focused on identifying the mobile elements and pseudogenes in the other Shewanella genomes, as they are completed. The results of these and others ongoing efforts will be used to develop a better understanding of how changes in environmental conditions lead to the evolution of new bacterial species and metabolic capabilities, with emphasis on those that might be harnessed for bioremediation purposes.

Acknowledgment: The research in this study was funded by DOE's Office of Biological and Environmental Research, Genomics: Genomes to Life Program. The Pacific Northwest National Laboratory advances scientific frontiers for U.S. competitiveness by achieving a predictive understanding of multi-cellular biological systems.

Research Team: The research team led by Margaret Romine included Tim Carlson, Angela Norbeck, Lee Ann McCue, and Mary Lipton, all of PNNL.